Notes: Drosophila’s View on Insect Vision (Borst, 2009)

Overview of Drosophilia’s Eyes and Visual Pathway

• Insect eyes are composed of repetitive units called facets.
• The eyes found in most insects can be categorized as apposition eyes or superposition eyes. In apposition eyes, the photoreceptors are isolated from each other within facets. In superposition eyes, which are often found in nocturnal insects, many facets act together without partitioning the photoreceptors. Here, apposition eyes will be focused upon.
• In the eyes of dipterans (flies), there are six photoreceptors (R1-R6) surrounding a stacked pair of central photoreceptors (R7-R8) within each ommatidium. Because of this arrangement, there are distinct axes along which light enters the photoreceptors in a single ommatidium.
• However, the photoreceptors in neighboring ommatidia take in light along parallel axes. The photoreceptors which receive light on parallel axes project to the same postsynaptic target.

• This kind of structure indicates that, unlike in some cartoons, insects do not see the world as “honeycomb pixels.” They form a unified neural representation of the environment. However, small dipterans like Drosophila (with fewer facets than larger insects like dragonflies) do have poor spatial resolution.
• Insect nervous systems generally include a head ganglion (brain), three thoracic ganglia, and several abdominal ganglia. However, Drosophila’s thoracic and abdominal ganglia are fused into a single thoracic ganglion.
• Drosophila’s thoracic ganglion is linked to the head ganglion via the cervical connective, a structure which contains about 3600 afferent and efferent axons.
• Drosophila’s head ganglion has a cortex composed of cell bodies which project inwards to form a structure called the neuropile. The neuropile consists of numerous fibers which synapse upon each other. (This kind of anatomical organization is common among all insects).
• The head ganglion in Drosophila is subdivided into the central brain, the subesophageal ganglion, and the primary sensory centers. The visual ganglia are among the primary sensory centers.

Visual Neuroanatomy in Drosophila

• Drosophila’s visual system is divided into three subcortical layers including the lamina, medulla, and the lobula and lobula plate. These structures form retinotopic maps and have repetitive columns.

• There is an optic chiasm (crossing of pathways from the two visual fields) from the lamina to the medulla and an optic chiasm from the medulla to the lobula complex.
• The central photoreceptors (R7-R8) project through the lamina and make synapses in the medulla. By contrast photoreceptors R1-R6 terminate in the lamina.
• The lamina column is called the cartridge. It contains lamina monopolar cells L1-L5, the centrifugal cells C1-C2, and the single T1 cell. All of these connect the lamina to different layers of the medulla. L1-L3 are postsynaptic to photoreceptors R1-R6.
• Every medulla column contains about sixty neurons. These neurons can be classified according to their anatomical connectivity.
  • The intrinsic medulla (Mi) neurons terminate within two or more layers of the medulla and do not send projections elsewhere.
  • Transmedulla ™ cells and bushy T2-T3 cells connect one or more layers in the medulla to the lobula.
  • Transmedulla Y-cells connect several layers within the the medulla to the lobula. Their axons bifurcate and project into both the lobula and the lobula plate simultaneously.
  • Bushy T4 cells connect the innermost layer of the medulla only to the lobula plate. The bushy T4 cells are called T4a-d depending on which layer of the lobula plate they terminate within.
  • The lobula and lobula plate are connected by bushy T5 cells. Some of the bushy T5 cells project into the most posterior layer of the lobula. The rest project into one of four layers in the lobula plate (and are called T5a-d depending on the layer).
  • In addition to columnar cells, there are many laterally oriented neurons in the medulla which form thin sheets perpendicular to the columns.
• Lobula plate tangential cells are a type of large neuron found in the lobula plate. The dendritic arbors of these cells are extensive enough that they can take inputs from thousands of different columns.

Drosophila Phototransduction

• Vertebrate photoreceptors hyperpolarize upon exposure to light and are active in dark conditions.
• By contrast, insect photoreceptors are depolarized under illumination.
• In addition, insect photoreceptors have more than three-fold higher temporal resolution than those found in vertebrates.
• Insect photoreceptors are densely packed along folded membranes which resemble microvilli. These membranes are called rhabdomeres.
• The rapid temporal response to light arises in large part from the high surface area of the rhabdomeres and the small distances required for signaling molecules to diffuse among the folds of membrane.

• Drosophila and vertebrates both transduce light using rhodopsin proteins with bound cofactors. While vertebrates carry the cofactor retinal, Drosophila instead uses a cofactor called 3-hydroxyl retinal. When exposed to a photon, this cofactor undergoes a cis-trans isomerization and the rhodopsin protein undergoes a conformational change to metarhodopsin.
• Insect meta-rhodopsin is stable and can easily convert back to rhodopsin without exchanging the cofactor molecule (unlike in vertebrates, which use a multistep process to exchange trans-retinal for cis-retinal and reset to rhodopsin).
• For Drosophila, phototransduction begins with the absorption of a photon by rhodopsin, which then converts into metarhodopsin. The metarhodopsin activates a G-protein. The G_α subunit then activates phospholipase C (PLC) which cleaves the phospholipid PIP₂ into IP₃ and diacylglycerol. These second messengers lead to the opening of calcium channels (which are called trp and trp-like). The resulting influx of calcium depolarizes the photoreceptors and triggers release of the neurotransmitter histamine (which is inhibitory in this context). Finally, calcium is rapidly removed by an antiporter protein called Sodium-Calcium exchanger (CalX).

 

References

Borst, A. (2009). Drosophila’s View on Insect Vision. Current Biology, 19(1). doi:10.1016/j.cub.2008.11.001

Montell, C. (2012). Drosophila visual transduction. Trends in Neurosciences, 35(6), 356-363. doi:10.1016/j.tins.2012.03.004